| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Departments of Physiology and Biophysics, Rehabilitation Medicine, and Regional Primate Research Center, University of Washington, Seattle, Washington 98195
 |
ABSTRACT |
|---|
 Abstract
 Introduction
Methods
Results
Discussion
References
|
|---|
Turner, Robert S. and Marjorie E. Anderson. Pallidal discharge related to the kinematics of reaching movements in two dimensions. J. Neurophysiol. 77: 1051-1074, 1997. Movement-related discharge of neurons in the internal and external segments of the globus pallidus (GPi and GPe, respectively) of two monkeys was studied during reaching movements in a two-dimensional workspace. Discharge was studied during movements to targets in eight directions and at three distances from the starting position under three behavioral conditions that manipulated target visibility and movement triggering. A total of 73 neurons (57 in GPe and 18 in GPi) with changes in discharge in concert with arm movements were included in a quantitative analysis. Of these, 83% also changed their discharge during manipulation of the contralateral arm outside of the task. Although 73% of changes in discharge began before the initiation of movement, they seldom preceded the initial activity of the agonist muscles. Decreases in discharge were more common than reported previously, constituting 40% of the changes in discharge detected. In GPi neurons, decreases also tended to begin earlier than increases. Changes in discharge in GPe neurons were of larger magnitude than those in GPi, and increases in discharge were larger than decreases. Onsets of changes in discharge were temporally linked to movement onset in 69% of neurons. Time locking of neural onsets to trigger presentation and movement termination was found in only 30 and 1% of neurons,respectively. Direction of movement influenced the magnitude of changes in discharge in 78% of cells. Directional modulations were broadly tuned and preferred directions were uniformly distributed across the range of directions. When directional modulations were large, preferred directions were consistent for different amplitudes of movement and for different behavioral conditions. Amplitude of movement influenced the magnitude of changes in discharge in 78% of cells, and in 80% of cases that relation had a significant linear component. Amplitude effects were not more common or stronger for movements in directions close to a cell's preferred direction. Linear relations to movement amplitude were more common and accounted for more of the trial-to-trial variance in discharge rate than relations to either average velocity or movement duration. The relation to movement amplitude was consistent for two behavioral conditions when the change in discharge was scaled strongly with movement amplitude. Movement-related changes in discharge of neurons in the skeletomotor portions of both pallidal segments reflect the kinematics of movement. This information, encoded in combination with sensory and contextual information, may play an on-line role in the selective facilitation and suppression of different frontal thalamocortical circuits.
The role of the basal ganglia in normal motor control remains unclear, although disorders of movement are the cardinal signs of parkinsonism and other conditions characterized by anatomic and biochemical changes in the basal ganglia. It is clear, however, that a subsection of the basal ganglia circuitry is devoted to somatomotor functions (Alexander et al. 1990 Animals and apparatus
Two juvenile male Macaca fascicularis monkeys, weighing 2.3-2.8 kg when obtained, were used in these experiments. Animals were cared for in accord with the Guiding Principles in the Care and Use of Animals (American Physiological Society, 1991). The monkeys were trained to perform three related visuomotor reaching tasks to obtain apple sauce or fruit juice rewards.
Behavioral tasks
Both animals were trained to make arm movements under three conditions designed to manipulate the cognitive requirements of a basic reaching task. The monkey was required to 1) hold the hand within the central start position zone for an initial hold period (H to T, "start position time," Fig. 1); 2) move its hand quickly to a specified target location at the end of the start position time (T to E, "response time"); and 3) hold its hand at the target location for
Sensory condition (Fig. 1E1)
Under the sensory condition, the target location was visible during the movement and the time at which movement was to be made was cued overtly. At the end of a start position time 1.5, 2, 2.5, or 3 s in duration, one of the target lights was illuminated and the trigger tone sounded simultaneously (T). Both the target position and the start position time were selected pseudorandomly. The monkey was required to move its hand to the target zone for the illuminated LED within 0.8 s and remain within the target zone for Precued condition (Fig. 1E2)
Under the precued condition, the target position was indicated in advance but was not visible during the movement, and a trigger tone was presented to signal movement initiation (M). One target light was presented (Q) for a short time (0.5 or 0.1 s) at 0.7 s after the beginning of the start position time. As in the sensory condition, the monkey was required to keep the hand in the start zone until the trigger tone sounded at the end of the variable start position time. Response time and target hold time were the same as in the sensory condition.
Self-timed condition (Fig. 1E3)
Under the self-timed condition a single peripheral target light and the central LED were both illuminated continuously and no trigger tone was presented. The monkey was required to initiate movement to the peripheral target within a time window of 1.5-3 s after acquiring the central start position. The permitted start position time was therefore roughly equivalent in range to the variable start position times of the other two conditions. After training, however, animals adopted start position times that were much less variable than under the other two conditions.
Surgery
After completion of training, a cylindrical stainless steel chamber (10 mm diam) was surgically implanted with the use of standard techniques (Anderson and Turner 1991b Neural recording
The activity of neurons in globus pallidus was recorded extracellularly as described previously (Anderson and Horak 1985 Sensorimotor examination
On completion of data collection in the behavioral tasks, the activity of all neurons was examined for responses during a detailed sensorimotor examination in which the experimenter manipulated the arm around the shoulder, elbow, forearm, wrist, and finger joints. The leg, back, tail, and neck were manipulated in a similar manner, and orofacial areas were explored by manipulating the inside of the mouth with a cotton swab soaked in applesauce. Neural activity was also evaluated while watching spontaneous eye movements and targeted eye movements to small bits of apple.
Data analysis
Data were digitized off-line at a 2-kHz sampling rate for each channel with the use of the ComputerScope ISC-67 system from RC Electronics (Santa Barbara, CA). Digitized channels included pulses from the spike discriminator, instantaneous firing frequency, behavioral logic signals, and X and Y arm position.
Detection of perimovement changes in discharge
Significant changes in discharge rate were detected in perimovement averages of a neuron's firing frequency. A "search period," extending from 300 ms before M until 200 ms after M, was tested for changes from the mean rate measured during a 500-ms control period ending 300 ms before M. The average firing frequency was considered to have a significant "movement-related change" if four of eight consecutive 5-ms bins in the search period were significantly above or below the baseline discharge rate (2-tailed t-test, 1 sample vs. baseline discharge mean, P < 0.02). The time of the first significant bin was taken as the onset time of a movement-related change in averaged discharge. The time of offset of a change in averaged discharge was detected in a similar way by searching the average after response onset for at least four of eight consecutive bins that were not significantly different from the control rate (P > 0.02). These detection criteria were arrived at by screening the efficacy of a wide variety of potential detection criteria applied to all perimovement averages for all cells studied. The present criteria were chosen because they allowed determinations, in a straightforward and nonbiased way, of the onsets of perimovement changes in discharge that were in close agreement with estimates based on visual inspection. All of the changes in discharge detected with the use of these criteria were of relatively large magnitude and long duration, with peak changes in discharge >3 SD away from the baseline discharge rate and durations>80 ms.
Measures of perimovement discharge
Maximum and minimum discharge rates were extracted for each valid trial from a perimovement epoch of smoothed frequency of firing data (300 ms before to 200 ms after M). The frequency of firing data for a single trial were low-pass filtered with a cutoff at 2.5 Hz with the use of a digital filter algorithm (Fig. 1A) (Hamming 1983 Movement direction effects
The relation of a cell's discharge to movement direction (directionality) was determined independently for increases and decreases in activity. Target direction, which correlated very closely with movement direction (Turner et al. 1995 Movement amplitude, velocity, and duration effects
The influence of the target distance on perimovement discharge was first tested with one-way analyses of variance (ANOVAs) (target distance vs. maximum and minimum discharge) for each direction in which targets were presented at three eccentricities from the start position. The nature of the relation between discharge and movement amplitude, target distance, and other correlated kinematic variables (MT or mean tangential velocity during movement) was explored with regression analysis. The linear model presented in Eq. 3 was tested with the use of least-squares regression (Systat)
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). Cells in the "motor" territory of the internal segment of the globus pallidus (GPi) carry basal ganglia output signals related to somatomotor activity (DeLong et al. 1985), and these neurons exert a direct inhibitory influence on target neurons in the ventrolateral thalamus and midbrain (Anderson and Turner 1991a; DeVito et al. 1980; Harnois and Filion 1982; Uno and Yoshida 1975). The activity of neurons in the motor territory of the external segment of globus pallidus (GPe) can also influence motor centers by way of inhibitory projections to the subthalamic nucleus, GPi, and the nucleus reticularis of the thalamus (Hazrati and Parent 1991; Hazrati et al. 1990; Kim et al. 1976). Thus movement-related signals carried by neurons in both GPi and GPe could influence movement execution via their indirect action on neurons of motor-related areas of the cerebral cortex or the brain stem.
; Anderson and Turner 1991b; DeLong 1971) and it is usually related to the movement of individual joints (Hamada et al. 1990). In some studies it was reported that movement-related changes in pallidal discharge are often influenced by kinematic and kinetic variables, including the direction of movement, the force being exerted, the movement duration (MT), and the amplitude and/or velocity of the movement (Anderson and Turner 1991b; Georgopoulos et al. 1983; Mitchell et al. 1987). Others, however, have reported that the relations of pallidal discharge to specific parameters of movement are weak and inconsistent across different task conditions (Brotchie et al. 1991a; Mink and Thach 1991b). Although a preferential relation of pallidal discharge to fast movements has been reported (Mink and Thach 1987, 1991b) and the magnitude of modulation may be enhanced during rapid movements, pallidal movement-related discharge is present during both fast and slow movements (Hamada et al. 1990).
). Reductions in GPi discharge are hypothesized to facilitate movement planning or execution by disinhibiting thalamic and brain stem targets. This action parallels that proposed for pauses in substantia nigra reticulata (SNr) discharge in facilitating saccadic eye movements (Hikosaka and Wurtz 1983c). In contrast, pauses in GPe discharge would suppress movements by increasing inhibition of the same targets via indirect pathways. Thus possible differences in the movement-related discharge of GPe and GPi neurons are of interest for models of basal ganglia function.
; DeLong 1971; Georgopoulos et al. 1983).
; Hikosaka and Wurtz 1983b; Mink and Thach 1991a; Mushiake and Strick 1995), we also have compared the discharge of individual pallidal neurons during similar movements made in different task contexts. We have found that GPi neurons have early decreases and late increases in discharge compared with the timing of changes in GPe discharge. The movement-related discharge of most pallidal neurons is related consistently to the direction of movement, irrespective of movement amplitude and task context. Relations of discharge to movement amplitude were also common. Preliminary results and an analysis of the task-related kinematics and electromyographic (EMG) activity have been presented previously (Turner and Anderson 1991; Turner et al. 1995).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
. Briefly, target light-emitting diodes (LEDs) could be illuminated and visible as virtual images in the workspace of the arm via a mirrorized sheet of Plexiglas positioned in front of the animal. Twenty-four peripheral targets were arranged in eight spokes separated by 45°, with the three targets in each spoke at 1, 2, and 3 in. from a center light. When the LEDs were not lit, their locations were not visible to the monkey.
).
0.4 s ("target hold time"). The monkey received a drop of apple sauce or fruit juice ("reward") on approximately half of the trials that were performed correctly.
View larger version (42K):
[in a new window]
FIG. 1.
Neural and kinematic data from 1 behavioral trial. A: instantaneous frequency of firing of neuron in the external segment of globus pallidus (GPe) as digitized (thin line) and after low-pass filtering (thick line). Raster marks below time axis: times of individual action potentials. Three small triangles below raster: from left to right, times of trigger presentation, movement onset, and movement termination. B: unprocessed extracellular recording of neural discharge from which frequency of firing (A) was calculated. C: tangential velocity of the hand, calculated off-line from hand X and Y position (D). D: X and Y position of the monkey's hand. E: schematic of event timings during the 3 behavioral conditions. E1: sensory condition. E2: precued condition. E3: self-timed condition. (See text for details.)
0.4 s.
15 valid trials for each target location were collected. If a trial was performed incorrectly, the target presented in that trial was presented again at the end of the sequence of trials. Self-timed trials were performed in multiple blocks with one peripheral target location visible continuously throughout a block. In most cases, a block of sensory condition trials was followed by blocks of precued and self-timed condition trials. Only then was a second block of sensory condition trials presented that used a different set of targets than presented in the first sensory block.
) to allow access to the globus pallidus from a 45° lateral approach (Szabo and Cowan 1984). The monkey was given Tylenol analgesic immediately after surgery and was allowed 2 days to recover before the first exploratory electrode penetrations.
; Anderson and Turner 1991b). The first neurons encounted had the low tonic firing rates typical of cells in the putamen (Crutcher and DeLong 1984a). The passage of the electrode into the pallidum was marked by a sharp increase in the background neural activity, and isolated action potentials characteristic of pallidal neurons were of short duration (~0.3 ms from onset of initial negativity to peak positivity) and had high tonic firing rates (DeLong 1971). Penetrations were placed initially in an 0.5-mm grid throughout the chamber, but the areas in which neurons with activity related to arm movement were encountered were sometimes explored on a finer grid.
), and tangential arm velocity was calculated with the use of Eq. 1
In Eq. 1, VX and VY are smoothed X and Y arm velocities and VT is the resulting tangential velocity.
(1)
). The filtering process preserved in the single-trial frequency of firing waveform the main features of changes in discharge observed in perimovement averages. These measures (maxima and minima) provided a way to analyze separately both components (increases and decreases) of the biphasic changes in discharge that were common for many pallidal neurons and were used for all subsequent analyses.
. Briefly, onset and offset times of a change in discharge (a "response") were shifted iteratively to find the epoch with a maximum difference between the distributions of response and control frequencies of firing. The control period extended from 800 ms before M to response onset. Onset times were allowed to shift between 300 ms before and 200 ms after M. Although onsets and offsets of multiple response phases could be detected with the use of this technique, only the onset times of the earliest increases and decreases in discharge are discussed in this paper.
; Hanes et al. 1995). If a neuron's discharge has a close temporal relation to M, then the time between the trigger and the neuron's initial change in discharge (onset-T) should covary with the behavioral reaction time (RT, the T to M interval). If, on the other hand, its initial change in discharge shows a tighter temporal linkage to the trigger, then the time between its onset and M (M-onset) should covary with the RT. To test for these linkages, Pearson product-moment correlations were calculated for the behavioral RT versus onset-T and M-onset.
), was used as the independent variable in statistical tests for directionality because of its discrete nature. Significant unimodal directionality in a cell's minimum or maximum perimovement discharge was determined with a nonparametric randomization test adapted from Lurito et al. (1991). First, mean resultant length, 
, was calculated for the absolute magnitude of a cell's dynamic increases and decreases in discharge (Fisher 1993; Mardia 1972). (Absolute dynamic changes in discharge were calculated as the absolute value of maximum or minimum discharge minus the neuron's baseline discharge rate.) The value is essentially the length of the vector sum of all target direction by discharge rate vectors, and its magnitude reflects the unimodal directionality of the data. A distribution of 5,000 "control" mean resultants was produced from random shufflings of the data, in which single-trial discharge rates were reassigned to one of the target directions selected at random. If the actual mean resultant, , was greater than the 95th percentile of the distribution of 5,000 control mean resultants, then the increase or decrease in discharge was considered to have a significant unimodal directionality (P < 0.05, approximate). The mean direction, 
, of a significant mean resultant was taken as the preferred direction of that increase or decrease in discharge. Because absolute changes in discharge from the control discharge rate were used in these calculations, preferred directions always reflected the direction in which the change in discharge was maximal, regardless of whether the change was an increase or decrease. The mean angular deviation, a circular equivalent to the SD, was calculated from the mean resultant and was used as a measure of the angular breadth of a cell's directional tuning (Fortier et al. 1993).
)
In Eq. 2,
(2)
is target direction (the independent variable), a is the baseline discharge rate of the cell (measured before T, as described above), and y is the predicted sinusoidal model of discharge rate. The coefficients resulting from this analysis reflect b, the mean change in discharge rate across all directions included in the analysis (i.e., offset); g, the half-wave amplitude of the sinusoidal function (i.e., gain); and Rpd, the direction in the sinusoidal function with a maximal change in discharge from the resting rate (e.g., regression preferred direction). The component of a perimovement change in discharge that was not modulated by movement direction (i.e., the unmodulated component) was estimated by subtracting the gain coefficient g from the offset coefficient b. This gave the difference in discharge from baseline rate to the point on the tuning curve closest to baseline firing. The coefficient of determination (R2) from the regression analysis was used as an estimate of how much of a cell's trial-to-trial variability in discharge could be accounted for by the cosine function.
In Eq. 3, D is the predictor variable and y is the predicted maximum or minimum discharge rate. Coefficients a and b represent the Y-intercept and slope (spikes·s
(3)
1·cm1) of the model.
Histology
Marking lesions were made at selected positions (e.g., presumed border between GPe and GPi, 1st location of optic tract activity) by passing DC (30 µA for 10 s) through the recording electrode.
| |
RESULTS |
|---|
|
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
Neurons sampled
The discharge of 293 pallidal neurons was monitored during a sensorimotor examination, 74 neurons in monkey F and 219 in monkey I. In agreement with previous studies (DeLong 1971; DeLong et al. 1985; Hamada et al. 1990), many of these (123 of those examined) responded to passive rotation or manipulation of one joint or body segment, often to very small movements of specific joints or palpation of selected muscles. Because the neurons documented in this study were those encountered during search for pallidal "arm" neurons and regions with these neurons were explored intensively, the numbers of neurons found responding to different body parts do not reflect the true proportions in the overall population of globus pallidus neurons.
Movement-related discharge under the sensory condition
Under the sensory condition, 73 of the 75 cells had significant movement-related changes in average firing rate around the time of M. The remaining 2 had movement-related discharge only under precued or self-timed conditions and will not be included in this description. The general characteristics of pallidal movement-related changes in discharge resembled previous descriptions (Anderson and Horak 1985
Influence of direction on perimovement discharge
Perimovement averages and rasters revealed directional modulations in movement-related discharge that were smoothly and broadly tuned for most pallidal cells. Figure 6A illustrates the movement-related discharge of a cell in GPe that responded to elbow manipulation and had a large decrease in discharge beginning as early as 100 ms before M. Rasters and averages for movements to targets at 2 in. from the start position are arranged according to the eight target directions. The decrease in discharge, although present for movements in all eight directions, differed in magnitude with movement direction (randomization test, P < 0.0004), with the maximum decrease accompanying movements directly to the left (preferred direction 183°).
Consistency of direction effects across movement amplitudes and behavioral conditions
When directional modulations in movement-related discharge were large, they also were consistent across different amplitudes of movement and under different behavioral conditions. Figure 10A shows, for one neuron with a movement-related decrease in activity, the mean minimum discharge during movements to targets in eight directions at 1, 2, and 3 in. from the start position. (Data for 0, 45, and 90° directions are plotted again at 360, 405, and 450° to aid illustration of the directional modulation.) This neuron's decrease in discharge, maximal during movements toward the monkey and to the right (270-405°), showed a consistent directionality across the three target distances. The preferred directions (indicated in Fig. 9A by 3
Influence of movement amplitude on perimovement discharge
There was a significant relation between movement amplitude (or target distance) and perimovement discharge rate in a high proportion of pallidal neurons. Figure 12 illustrates an example of this for a neuron in GPi. Data are plotted for movements made to targets at 1, 2, and 3 in. directly to the left and right of the start position (left and right columns). The average movement trajectories are shown in the middle. During movements to the left, this neuron had an increase in firing rate that began at about the time of M and became smaller in peak magnitude as movement amplitude increased. The discharge remained above control values after movements to the left were completed (during the target hold time), but the magnitude of this sustained discharge was not influenced by the distance of the target from the start position. During movements to targets to the right of the start postion, the neuron had a small but consistent decrease in firing rate, but its magnitude was not influenced perceptibly by the amplitude of movement.
Consistency of amplitude effects across behavioral conditions
When there was a strong relation between perimovement discharge and movement amplitude, the effects of movement amplitude were similar under the sensory and precued conditions. Figure 17A shows an example of similar movement amplitude effects under sensory and precued conditions in data from a GPe cell. Maximum perimovement discharge rate on single sensory and precued trials (
The current results show that, when the perimovement discharge of pallidal neurons was evaluated during multijoint arm movements made in several different directions, movement-related changes in discharge were directionally modulated. Changes in discharge also varied with movement amplitude or a kinematically related characteristic of the movement. The directional modulation was broadly tuned, and it was consistent for different amplitudes of movement and for movements made under different behavioral conditions. Movement amplitude-related changes in activity were not restricted to a cell's preferred direction, nor were they distributed across all directions in a manner that would shift the entire directional tuning curve. When movements were made to visible versus remembered target locations, the magnitude of a cell's movement-related change in discharge was often different. When that movement-related change was scaled strongly with movement amplitude, however, amplitude scaling was similar across different behavioral conditions.
Form and timing of changes in pallidal discharge
The current study reveals a higher incidence of initial decreases in the discharge of pallidal neurons than was reported in other studies of limb movement. In the oculomotor-related portion of the substantia nigra, neurons with axons directed to the superior colliculus have a reduction in discharge in association with saccadic eye movements (Hikosaka and Wurtz 1983a Movement direction
The incidence of significant directionality in the discharge of 78% of the pallidal neurons studied is much higher than has been reported in other studies, all of which used movements restricted to one dimension and often to one joint. Georgopoulos et al. (1983) Movement amplitude
Movement-related changes in pallidal discharge commonly varied not only with movement direction but also with movement amplitude. Amplitude-related changes in pallidal discharge during the movement time also were reported for a large percentage of the cells studied by Georgopoulos et al. (1983) Role(s) of pallidal discharge in motor control
Several roles have been proposed for the basal ganglia, especially with respect to motor function. Hikosaka and Wurtz, who examined the role(s) of the basal ganglia with respect to saccadic eye movements, proposed that the reduction of activity in oculomotor-related cells of SNr facilitated (by disinhibition) the saccade-related burst of discharge in cells of the superior colliculus and resulted in earlier saccades of increased velocity (Hikosaka and Wurtz 1983c We thank B. Bedell for excellent technical assistance, Dr. Warren Smith for computer programming, and Dr. John Buford for helpful comments.
Address for reprint requests: R. S. Turner, Dept. of Neurology, WMRB 6000, Emory University, Atlanta, GA 30322. Received 2 July 1996; accepted in final form 29 October 1996.
View larger version (17K):
[in a new window]
FIG. 2.
Location of neurons studied in GPe and the internal segment of globus pallidus (GPi) of 2 monkeys. A: monkey F. B: monkey I. Filled circles: pallidal arm responsive neurons included in the quantitative analysis. Circles with crosses: nonresponsive "near-arm" neurons included in the quantitative analysis. Open circles: arm responsive neurons not included in analysis. Small dots: neurons responsive to manipulation of other body segments or unresponsive and not included in the study.
; DeLong et al. 1985; Mitchell et al. 1987). Significant increases were detected in the discharge of 88% of the cells (64 of 73) for at least one movement direction, and decreases were detected in 66% (48 of 73). In about half of the cells, both increases and decreases in discharge were found (39 cells, 53%) consisting of biphasic changes in discharge (32 cells) or pure increases in discharge for some target directions and pure decreases for other directions (7 cells). The remaining 34 cells had only increases (25 cells) or decreases (9 cells) in discharge. Overall, across all directions tested in every cell, 60% of the detected changes in discharge were increases and 40% were decreases.
60 ms) (Turner et al. 1995). Although the latency distributions for increases and decreases overlapped nearly completely, the distribution for decreases was skewed toward earlier onset times (medians: 50 and 40 ms for decreases and increases, respectively), and the two distributions were significantly different (Komolgorov-Smirnov 2-sample test, P < 0.03).
View larger version (20K):
[in a new window]
FIG. 3.
Distribution of onsets of initial perimovement changes in discharge including all changes detected (i.e., multiple target directions per neuron). Distributions for increases and decreases in discharge are plotted above and below the 0 axis, respectively. A: distributions of onsets for all pallidal neurons. Binwidth: 20 ms. B: cumulative distributions of onsets for GPe ( 
) and GPi (- - -) neurons.
View this table:
TABLE 1.
Timing of changes in discharge
2 test, P > 0.3). When biphasic changes in discharge were detected, however, a decrease in discharge was the first change in nearly all GPi discharge (i.e., the "/+" type accounted for 14 of 15 cases, 93%). Increases began the majority of biphasic changes in GPe discharge ("+/" type accounted for 22 of 39 cases, 56%). This constituted a significant difference between GPi and GPe neurons in the incidence of /+-type biphasic changes (2 test, P < 0.001).
55 ms, which was followed by an increase starting at +35 ms. In contrast, the population average for GPe neurons (Fig. 4, ) showed only an increase in discharge starting at 75 ms.
View larger version (28K):
[in a new window]
FIG. 4.
Population averages of perimovement discharge for all GPe( ) and GPi (- - -) neurons. Averages include data from each neuron for all target directions in which a perimovement change in discharge was detected. Each neuron's baseline discharge rate was subtracted from individual averages before averaging across directions and neurons.
) was relatively constant and showed no correlation with RT, whereas the onset-T interval (Fig. 5B, 
) showed a positive correlation with RT (Pearson product-moment correlation, P < 0.001).
View larger version (38K):
[in a new window]
FIG. 5.
Example of the temporal linkage to movement onset of the onset of a perimovement change in discharge. A: average perimovement discharge and rasters aligned on movement onset (vertical dotted line, 0 ms). Baseline discharge rate (56.4 spikes/s) is indicated by a horizontal dotted line through the average. Rasters are sorted in order of increasing trigger (left triangle in each row) to movement onset interval (reaction time). B: interval from trigger presentation to the onset of the change in discharge ( ) was correlated strongly with reaction time. The interval from neural onset to movement onset (), however, was relatively constant and independent of reaction time.
View larger version (72K):
[in a new window]
View larger version (53K):
[in a new window]
FIG. 6.
Examples of direction-related modulations in the perimovement changes in discharge of 2 pallidal neurons. A: and B: records for 2 GPe neurons. Average frequency of firing and rasters of neural discharge for 8 classes of trials are arranged according to the target direction presented on those trials. Averages and rasters are aligned on the time of movement onset (0 ms), and rasters are sorted according to increasing reaction time. The average tangential velocity profile for each set of trials is superimposed as a thin line on each frequency average. Abscissas: ms relative to the onset of movement. Ordinates: spikes/s. Calibration tick mark at the right of each average: 150 spikes/s and 25 cm/s. Average hand trajectories are shown for each target direction in the middle of both panels. Thick lines: X vs. Y hand position. Plus signs: target locations. Asterisks: center light position. Open circles: average positions of hand during center hold period for each target direction.
) was only slightly modulated with movement direction, compared with the dramatic directional modulation of the later increase (
). The randomization test found a slight directionality in the early decrease (0.02 < P < 0.05, preferred direction at 223°), whereas the directionality of the late increase was highly significant (P < 0.0004, preferred direction at 89°). Cosine functions (Fig. 7, solid lines) accounted for 69% of the trial-to-trial variance in this cell's perimovement increases, but only 6% of the variance in decreases.
View larger version (15K):
[in a new window]
FIG. 7.
Examples of the directional tuning of mean change discharge rates. A: mean maximum and minimum discharge rates from data shown in Fig. 6B. B: mean rates for GPe neuron with significant directional modulations in both mean maximum and minimum discharge rates. Mean maximum ( ) and minimum () discharge rates for each of 8 target directions. Error bars: means ± SE. Solid curves: best-fit cosine functions. Arrows: preferred directions. Horizontal dotted lines: baseline discharge rates.
2 test, P < 0.06).
View larger version (17K):
[in a new window]
FIG. 8.
Population directional tuning curves for increases (A) and decreases (B) in discharge. Tuning curves for neurons with significant directional modulations in discharge were aligned on their preferred directions and averaged separately for GPe (circles) and GPi (triangles) neurons. Horizontal lines: mean baseline discharge rates for the GPe (solid) and GPi (hatched) neurons included in the population averages.
View larger version (29K):
[in a new window]
FIG. 9.
Angular distribution of preferred directions. A: distribution of preferred directions for increases and decreases in discharge. B: distribution of preferred directions for decreases in discharge relative to the preferred direction for increases in neurons that had significant directional modulations for both increases and decreases in discharge.
s) differed by only 9.9° when the deviation of the three preferred directions from equality was computed as the distance in three dimensions (1 in. vs. 2 in. vs. 3 in.) between the observed preferred directions and the line representing equality (1 in. = 2 in. = 3 in.).
View larger version (25K):
[in a new window]
FIG. 10.
Examples of similar preferred directions for different movement amplitudes and different behavioral conditions. A: mean minimum discharge rate in 1 neuron for movements to targets at 1 in. (squares), 2 in. (circles), and 3 in. (triangles) from the start position in each of 8 directions. B: mean maximum discharge rate in a different neuron for movements to targets presented in different directions under the sensory (squares, 8 directions), precued (circles, 6 directions), and self-timed (triangles, 3 directions) conditions. Data for directions of 0-45° are repeated at directions of 360-450° to aid depiction of directionality. Horizontal dotted lines: baseline discharge rates. Arrows: preferred directions, 1 for each of the tuning curves.
View larger version (34K):
[in a new window]
FIG. 11.
Comparison of preferred directions across movement amplitudes and behavioral conditions in the population of pallidal neurons. A and C: preferred directions for each directional change in discharge observed during movements to targets at 3 distances (A), and during movements to the same targets but under 3 behavioral conditions (C). Filled circles: preferred directions for increases in discharge. Open circles: preferred directions for decreases in discharge. Data are included in C only for changes in discharge that were significantly directional under all 3 conditions. B and D: relationship between the magnitude of directional modulation in discharge and the difference between preferred directions (distance from equality in 3 dimensions) across amplitudes (B) and conditions (D). When preferred directions were dissimilar, the directional modulation in discharge tended to be small. Changes in discharge with the largest directional modulations in discharge also had preferred directions that differed by <45° (filled circles).
near 270°). The perimovement discharge had significant directionality under all three behavioral conditions in 47% of the cases examined (21 of the 45 cases in which all conditions were presented and a directional change in discharge was detected). A plot of the preferred directions of these 21 cases (Fig. 11C) shows that preferred directions were similar under the three conditions.
View larger version (45K):
[in a new window]
FIG. 12.
Example of an amplitude-related modulation in the perimovement discharge of a GPi neuron. Averages and rasters of the discharge for movements to targets at 1, 2, and 3 in. from the start position (top, middle and bottom rows, respectively) in target directions directly to the left (left column) and right (right column) of center. Middle: average hand trajectories. Other conventions are same as in Fig. 6.
2 test). As was the case for target direction, increases in discharge were more often affected by target distance than were decreases (51% of increases and 38% of decreases).
), the maximum perimovement discharge was inversely related to movement amplitude, and this relation was approximately linear, with a slope of -8.6 spikes·s1·cm1 (least-squares linear regression, P < 0.001, R2 = 0.42). The neuron's discharge did not change with movement amplitude, however, when movements of similar amplitude were made to the right (0°, ).
View larger version (20K):
[in a new window]
FIG. 13.
Examples of the near linear relations between movement amplitude and perimovement changes in discharge. A: mean maximum discharge vs. mean movement amplitudes for movements to the left ( ) and right () for records shown in Fig. 12. B: mean minimum discharge rates of a GPe neuron for movements of different extent to targets in directions of 0, 45, and 135°. Lines from least-squares regressions are shown for each data set. Error bars: means ± SE.
View this table:
TABLE 2.
Frequency of significant amplitude-related effects as a function of the number of target directions studied
View larger version (28K):
[in a new window]
FIG. 14.
Mean changes in discharge vs. mean amplitudes of movement for the sample of increases and decreases in discharge that were positively (A) and negatively (B) correlated with movement amplitude. Population averages were computed for GPe and GPi neurons separately (circles and triangles, respectively). Relations to the extent of movement were similar for increases and decreases in discharge (filled and open symbols, respectively), for changes in discharge that were positively and negatively correlated with movement extent, and for neurons in GPe and GPi.
View larger version (35K):
[in a new window]
FIG. 15.
Distribution of target directions with amplitude-related modulations in discharge relative to the preferred directions of GPe (A and B) and GPi (C and D) neurons. A and C: relations of target direction tested relative to a cell's preferred direction (abscissa) and the slope of the regression line (ordinate). Open circles and triangles: increases and decreases in discharge, respectively, that had significant amplitude-related modulations. Dots: cases with nonsignificant regressions. B and D: cumulative angular distributions of target directions in which significant amplitude-related modulations were found relative to a cell's preferred direction (thick lines). These were not significantly different from the cumulative distributions of all target directions tested (thin lines).
; Georgopoulos et al. 1983).
2 test, P < 0.06).
View larger version (21K):
[in a new window]
FIG. 16.
Comparison of the linear relations between modulations in discharge and movement amplitude, movement velocity, and movement duration. The coefficients of determination (i.e., the proportion of variance accounted for, R2) for linear regressions of discharge onto movement amplitude (abscissas) are plotted vs. those for regressions onto average velocity or movement duration (ordinates in A and B, respectively). Points are plotted for all cases in which either regression was significant. Points below the diagonal dotted lines (which denote equal R2 for both regressions) indicate cases in which a change in discharge was more closely related to movement amplitude.
and , respectively) is plotted versus amplitude of movement. The slopes of the regression lines plotted for each condition did not differ significantly between the two conditions (6.2 and 5.6 spikes·s1·cm1 under sensory and precued conditions, respectively; F test, P > 0.5). The regression Y-intercepts were significantly different, however (150.9 and 127.8 spikes/s respectively, F test, P < 0.05), indicative of a larger movement-related change in discharge under the sensory condition that was not influenced by the amplitude of movement.
View larger version (22K):
[in a new window]
FIG. 17.
Relations of discharge to movement amplitude under 2 behavioral conditions. A: example of maximum discharge rates on individual trials performed under the sensory ( ) and precued () conditions for movements to targets in 1 direction at 3 distances from the start position. Linear regressions for the 2 conditions yielded lines with similar slopes but different Y-intercepts. B: slopes of regression lines for amplitude effects under the sensory condition (abscissa) plotted vs. those under the precued condition (ordinate). When discharge was modulated significantly with movement amplitude under both behavioral conditions (), regression slopes tended to be similar and of large amplitude.
). These were the cases in which regression slopes were large (3.35 and 3.33 spikes·s1·cm1 mean absolute slopes in sensory and precued conditions, respectively), and in most cases the slopes did not differ under the two conditions (71%, 5 of 7 cases). In one case, however, the slopes had opposite signs under the two conditions.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Reduced nigral inhibition is believed to facilitate the saccade-related bursts of discharge in collicular cells (Hikosaka and Wurtz 1983c). In contrast, studies of pallidal activity associated with arm movement always have shown a strong majority of initial increases in discharge (Anderson and Horak 1985; DeLong 1971; Georgopoulos et al. 1983; Mitchell et al. 1987). The incidence ratio of movement-related increases to decreases detected in perimovement pallidal discharge has been reported to be as low as 2.4 (Mink and Thach 1991b) and as high as 4.2 (Georgopoulos et al. 1983). In the current study, increases were only 1.56 times as common as decreases across all movement directions tested in all cells.
), as for nigral influences on eye movement, is that this reduction in GPi discharge would facilitate movement.
). The heavy preponderance of limb movement-related increases in GPi discharge reported in previous studies led to the conclusion that the main action of movement-related GPi discharge is to increase the inhibition of thalamocortical circuits and thereby suppress unwanted or inappropriate muscle excitations or reflexes (Mink and Thach 1991c). Why such phasic suppressive actions would not also be required by the SNr-superior colliculus saccadic control system remains unclear. It is possible that the large and variable loads encountered during limb movements but not in eye movements, which place additional requirements on skeletomotor control systems, give rise to such phasic increases in pallidal discharge.
). The median onset time for decreases in pallidal discharge was 50 ms before movement (55 for GPi alone), and for increases it was 40 ms before movement onset. This near concurrence between the initial change in pallidal and muscle activity was also the case in the studies of Nambu et al. (1990), Anderson and Turner (1991b), and Mink and Thach (1991b). One study of pallidal discharge reported onset times for movement-related pallidal discharge that were ~60 ms later than those found here (Georgopoulos et al. 1983). Differences in the behavioral task employed and analysis techniques may account for that difference.
; Hanes et al. 1995). Such a linkage does not indicate a direct causal relationship (e.g., that the onset of neural discharge contributes to M). It implies strongly, however, that the change in discharge is initiated by processes that are related more closely to development of the movement than to E. The prolonged duration of increases in discharge for larger-amplitude movements, which also usually have longer durations (unpublished observations), does open the possibility that the termination of the movement-related change in discharge is linked, in some way, to E. Because changes in pallidal activity also were seldom linked to T, this implies that they were seldom involved in the early stages of visuomotor transformation.
, who studied the activity of individual pallidal neurons during two directions of movement of a handle that the animal grasped (either push-pull or side-to-side), found directionally different activity in 48% of the cells in GPe and 56% of those in GPi. Mitchell et al. (1987), whose task restricted movements to flexion and extension around the elbow, reported that 30% of the pallidal neurons in both GPe and GPi had direction-dependent changes in firing. Mink and Thach (1991b) and Hamada et al. (1990) both used wrist flexion/extension tasks, and the former study reported directionally different movement-related discharge in 28% of the cells in GPe and 41% in GPi, whereas the latter reported only that movement-related changes in discharge were quite similar for wrist flexions and extensions.
), two-joint movements made by the two animals whose pallidal activity is reported here (monkeys F and I) had generally straight trajectories and single-peaked velocity profiles, and EMG activity in muscles acting at the shoulder (anterior and posterior deltoid and pectoralis) had directionally tuned changes in both the magnitude and the time of onset. Both the discharge of pallidal neurons and the EMG tuning curves for shoulder muscles were broad and fit well by a cosine function. Such broad neuronal tuning curves imply that in the one-dimensional tasks used by others, movements in opposite directions could easily be associated with similar neuronal discharge rates.
). There are also demands in multijoint movements for postural stabilization and compensation for dynamic interactions that are not present in single-joint movements (Gordon et al. 1994). It is possible that the discharge of pallidal neurons varies with movement direction because it plays a role in joint stabilization or inertial compensation, both of which change with movement direction.
), movements in this task are associated with directionally graded changes in both the amplitude and the timing of bursts of muscle activity in anterior deltoid, posterior deltoid, and pectoralis. Smaller EMG bursts in biceps and brachialis, which cross the elbow, showed smaller directional gradation in both amplitude and timing. Previous studies have found that a higher proportion of neurons in the somatomotor portions of the putamen and pallidum responds to manipulation of the proximal (shoulder or elbow) joints than to distal (wrist or finger) stimulation (Crutcher and DeLong 1984a; DeLong et al. 1985; Hamada et al. 1990). Any pallidal neuron whose discharge is influenced by movement at either the shoulder or the elbow joint, then, might be expected to have a directional variation in movement-related activity.
; Nambu et al. 1990). It is reasonable to expect that neurons in the pallidal territory that is influenced by primary motor cortex/primary somatosensory cortex would respond most frequently to passive movement of arm joints and/or muscle palpation (Flaherty and Graybiel 1993). These are the cells that were sought in the current study. Although DeLong and collegues (Georgopoulos et al. 1983; Hamada et al. 1990; Mitchell et al. 1987) also focused on pallidal neurons that responded to manipulation of the arm, others have studied populations that seldom responded to sensory stimulation of the arm (e.g., Brotchie et al. 1991a; Mink and Thach 1991a).
; Georgopoulos et al. 1982; Kalaska et al. 1989; Schwartz et al. 1988), premotor (Fu et al. 1993), and posterior parietal cortex (Kalaska et al. 1983, 1990). All of these cortical areas are sources of input to the putamen, and thus to the portions of the globus pallidus in which most of the neurons examined in the current study were located. Although addition of higher harmonics to the regression equation, which allowed the width of peaks and valleys in the turning curve to vary, sometimes improved the fit significantly, the width of the peaks still ranged from 90 to 270° and centered on the 180° width that characterizes a cosine function (unpublished observations).
). In addition, the fewer the directions sampled, the more inaccurate the determination of a cell's preferred direction. Thus many of the cases in which preferred directions did not agree across changes in behavioral condition, in this and in other studies, may be accounted for by errors introduced by limited sampling and by relatively small directional modulations in discharge.
also observed that, although the magnitude of a change in discharge was commonly modulated with movement direction, there was seldom a reciprocal change in discharge around the baseline discharge rate for opposing movement directions.
) or permanent (Horak and Anderson 1984a), do not result in changes in the trajectory or accuracy of targeted movements. Likewise, phasic stimulation of the pallidum during reaching movements commonly influences the speed of movement but does not alter movement trajectory (Horak and Anderson 1984b). It is more likely that the discharge of a pallidal cell contributes especially to some other aspect of motor control for movements made in particular directions.
; Filion et al. 1988; Hamada et al. 1990). Therefore the directional modulation in a pallidal neuron's discharge may have been linked to the direction and extent of rotation of the cell's specific joint. A recent study of neural discharge in primary motor cortex and parietal and premotor cortices during similar movements with the use of different arm postures suggests that the rotation of specific joints is represented in those areas as well (Scott and Kalaska 1995; Scott et al. 1995). At the other end of the spectrum of possible covariates, some neurons in the somatomotor putamen have task-related discharge that is related to the direction of the target or goal of the movement, independent of the direction of movement (Alexander and Crutcher 1990). Although the percentage of neurons in the putamen that responded in this way was low, at least some of the pallidal neurons in the present study may have had directional modulations in discharge that were related to the direction of the target and not to the direction of movement. In the present study, as well as in nearly all studies of the directionality of movement-related discharge in cortical neurons (Fu et al. 1993; Georgopoulos et al. 1982; Kalaska et al. 1983, 1989, 1990; Schwartz et al. 1988), target direction and movement direction were not dissociated.
(66% of the cells in GPe and 79% of those in GPi). That task involved multijoint push-pull or side-to-side movements of the entire arm, but it only examined amplitude scaling in two directions along one dimension. Although a similar incidence of significant linear amplitude scaling was found in the current study when only two directions were studied, all cells studied during movements in six or more target directions showed significant linear amplitude scaling during movement in at least one direction.
. Mink and Thach (1991b) and Brotchie et al. (1991a) both used tasks restricted to flexion/extension of the wrist and both searched for relations of pallidal discharge to movement amplitude that were independent of other aspects of task performance. Mink and Thach (1991b) dissociated the amplitude and velocity of wrist flexion/extension movements by the use of two target distances with two different target sizes. (Movements to small targets were slower than those to large targets at the same distance.) Twenty-one percent (7 of 34) of globus pallidus neurons showed significant correlations between movement amplitude and peak change in discharge. Brotchie et al. (1991a) used both different amplitudes of wrist flexion or extension movements and similar-amplitude movements that started from different initial positions to test for relations of pallidal discharge to the extent of movement that were independent of the movement start and stop positions. In only 29% of the 92 pallidal neurons studied was the discharge influenced by the amplitude of movement independent of start position, and in only 13% was that relationship linear. Both studies rejected the hypothesis that movement-related changes in pallidal discharge commonly reflect the amplitude of movement independent of other task factors.
). 3) Finally, if amplitude effects occurred only at specific points in a directional tuning curve, they could sharpen or broaden the width of the peaks or valleys in the directional tuning curve. This type of interaction would arise, for instance, if a neuron discharged according to the proximity of a movement's endpoint to a specific target zone or "movement field" in the workspace (Hikosaka and Wurtz 1983a,b). In the present study and in a study of motor cortices by Fu et al. (1993), the distribution of directions in which amplitude scaling was identified did not exclusively fit any of these models. Although individual neurons might signal the combined amplitude and direction of movement according to any one of the schemes outlined above, the limited number of directions consistently tested for amplitude effects in the current study precludes the categorization of most individual cells' discharge to one or another of these response types.
], we found that the relation between movement amplitude and peak change in a pallidal neuron's discharge was frequently consistent across different behavioral conditions. Thus the movement-related discharge of a pallidal neuron is usually influenced by a combination of task factors, but the amplitude of movement or some covarying movement or target parameter is a frequent component of that combination.
), the magnitude and duration of the force impulse produced to initiate the movement (Schmidt et al. 1979), the duration of the EMG burst in the agonist muscles (Buneo et al. 1994), the somatosensory consequences of the movement, and the target position (Alexander and Crutcher 1990). In the current study we provide evidence that pallidal discharge was more closely related to movement amplitude than to movement velocity or MT. Mink and Thach (1991b) also found a smaller percentage of pallidal neurons with significant correlations between peak change in discharge and peak movement velocity (6%) than with movement amplitude (22%). Brotchie et al. (1991a) reported that movement amplitude and velocity were not dissociated during the targeted movements, and they did not determine the relation between discharge and movement velocity quantitatively. They did, however, report that there was no relation between the magnitude of neuronal discharge and the velocity of oscillatory movements made at the final hold position.
; Crutcher and DeLong 1984b; Mitchell et al. 1987). The discharge of neurons in both putamen and the pallidum was often influenced by task loading conditions (i.e., whether an external load opposes or assists a movement), but the pattern of neural activity is seldom the same as the pattern seen in the activity of muscles used in the task (Crutcher and Alexander 1990; Liles 1985; Mitchell et al. 1987).
; Riehle et al. 1994). All of these cortical areas project to the somatomotor portion of the putamen and may contribute to the movement amplitude-related modulations in pallidal discharge.
). Mink and Thach, who examined the role(s) of the basal ganglia with respect to targeted wrist movements, proposed that perimovement increases in the inhibitory output of the basal ganglia suppressed the maintained activity in muscles that would oppose movement and allowed other mechanisms to generate a volitional limb movement (Mink and Thach 1991c). Although these two models disagreed concerning the sign of the change in discharge that facilitates movement, they both proposed an on-line consequence on movement kinematics of the facilitatory and/or suppressive effects of changes in output from the basal ganglia. Both also reported differences in the magnitude or importance of basal ganglia output in different task conditions.
; Houk and Wise 1995). The functional role of such basal-ganglia-mediated facilitations and suppressions would vary between different basal ganglia/frontal cortical circuits (Alexander et al. 1990). Whereas changes in discharge in pallidal neurons belonging to the prefrontal circuits may modulate response learning, working memory, or other proposed prefrontal cortical functions (Goldman-Rakic 1994; Passingham 1993), similar changes in pallidal neurons belonging to the motor circuit (Hoover and Strick 1993) may produce context-dependent modulations of movement execution.
, a new context is registered in a binary all-or-nothing way by self-sustained changes in the activity of corticothalamocortical loops. Such changes in the activity of thalamocortical motor circuits, the consequence of perimovement changes in discharge in basal ganglia output neurons, could bias the motor system to greater or lesser activation. However, they would not necessarily influence the movement in progress in an analog and on-line manner (Houk and Wise 1995).
; Horak and Anderson 1984b). Brief stimulus trains applied in the globus pallidus during the RT slowed the ensuing movement only if the train overlapped the time period 100-150 ms before M. Stimulation earlier or later than this critical period did not produce a change in movement time. A perimovement change in the pallidal inhibition of recipient thalamocortical or brain stem circuits must, then, be able to modulate on-line movement execution under at least some behavioral conditions. Although movement-related changes in pallidal activity recorded in this and other studies usually began too late to be involved in M, they did occur sufficiently early to influence the execution of an ongoing movement. These changes in discharge were not so late that they could only influence subsequent movements by a change in motor set, for example.
observed, after injection of muscimol into the SNr, that monkeys were unable to maintain constant visual fixation of a target because of "saccadic jerks." Hore and Vilis (1980), Mink and Thach (1991c), and Inase et al. (1995) all reported that reversible or permanent inactivation of GPi produced a drift of the arm around the joints that were free to move. As shown in the latter study, this was an active drift, accompanied by EMG activity of the agonists. When a cue indicated to the animal that the hand had drifted off the target zone, the EMG activity that contributed to the drift was terminated and the hand was returned to the target zone. This produced an oscillatory movement of the limb, similar to that of a saccadic jerk. Thus one consequence of the normal high level of inhibition of basal ganglia targets by neurons in movement-related portions of the globus pallidus or substantia nigra is positional stability. Concurrent with the period in which positional drift of the arm occurred, the tonic discharge rate of neurons in pallidal-receiving areas of the thalamus was increased (Inase et al. 1995). One might assume that the transient reductions in discharge present in some pallidal neurons under normal conditions would have similar facilitatory effects on their recipient thalamocortical circuits. Thus the facilitation of pallidal recipient circuits, either by normal transient reductions in pallidal discharge or by experimental inactivations of pallidal discharge, may promote a positional instability that allows movement to occur.
). In contrast, when neurons in motor regions of the globus pallidus were inhibited or destroyed, the velocity of arm movements was consistently reduced and antagonist muscles in the arm showed a pattern of cocontraction (Inase et al. 1995; Mink and Thach 1991c). It is not clear whether changes in velocity after disruption of basal ganglia output are due to a loss of phasic, movement-related changes in the discharge of pallidal or nigral neurons, and/or due to changes in the tonic activity of basal ganglia receiving circuits (Inase et al. 1995). The apparent conflict between the oculomotor and skeletomotor studies, however, may be accounted for by the different characteristics and roles of the two circuits. Saccadic eye movements are achieved by a burst of activity in the agonist extraocular muscles that is matched to the mechanical properties of the oculomotor plant, such that a burst of activity in the antagonist muscle is not required to terminate the movement accurately (Robinson 1970). Rapid targeted arm movements, however, are typically achieved by alternating bursts of activity in agonist and antagonist muscle groups (Turner et al. 1995; Wadman et al. 1980). A cocontraction of muscles acting antagonistically around joints also is commonly used to stabilize the limb against external perturbations. When drift of the limb is induced by injection of muscimol into GPi, the enhanced cocontraction observed in muscles across the joint may be a strategy adopted by the monkey to stabilize the limb and reduce the drift at the cost of slowing intended movement. Such a stabilizing agonist-antagonist cocontraction strategy may not be available in the oculomotor control system. Thus, with GPi inactivations, slowed limb movements could be a consequence of the attempt to maintain a stable position rather than a primary defect in the ability to activate a motor signal or command to produce a rapid movement.
; Hikosaka and Wurtz 1983b; Mink and Thach 1991a; Mushiake and Strick 1995). Although basal ganglia "function(s)" must thus be understood as the consequence of a basal ganglia outflow that reflects processed combinations of motor, sensory, and contextual information, the present study demonstrates that kinematic information is an important and consistent determinant of the outflow from skeletomotor-related portions of the basal ganglia.
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
Abstract
Introduction
Methods
Results
Discussion
References
0022-3077/97 $5.00 Copyright ©1997 The American Physiological Society
This article has been cited by other articles:
|
|
 |
|
  K. W. McCairn, M. Bronfeld, K. Belelovsky, and I. Bar-Gad The neurophysiological correlates of motor tics following focal striatal disinhibition Brain, August 1, 2009; 132(8): 2125 - 2138. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. W. McCairn and R. S. Turner Deep Brain Stimulation of the Globus Pallidus Internus in the Parkinsonian Primate: Local Entrainment and Suppression of Low-Frequency Oscillations J Neurophysiol, April 1, 2009; 101(4): 1941 - 1960. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Joshua, A. Adler, B. Rosin, E. Vaadia, and H. Bergman Encoding of Probabilistic Rewarding and Aversive Events by Pallidal and Nigral Neurons J Neurophysiol, February 1, 2009; 101(2): 758 - 772. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Elias, Y. Ritov, and H. Bergman Balance of Increases and Decreases in Firing Rate of the Spontaneous Activity of Basal Ganglia High-Frequency Discharge Neurons J Neurophysiol, December 1, 2008; 100(6): 3086 - 3104. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Desmurget and R. S. Turner Testing Basal Ganglia Motor Functions Through Reversible Inactivations in the Posterior Internal Globus Pallidus J Neurophysiol, March 1, 2008; 99(3): 1057 - 1076. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. F. Chang, R. S. Turner, J. L. Ostrem, V. R. Davis, and P. A. Starr Neuronal Responses to Passive Movement in the Globus Pallidus Internus in Primary Dystonia J Neurophysiol, December 1, 2007; 98(6): 3696 - 3707. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Nevet, G. Morris, G. Saban, D. Arkadir, and H. Bergman Lack of Spike-Count and Spike-Time Correlations in the Substantia Nigra Reticulata Despite Overlap of Neural Responses J Neurophysiol, October 1, 2007; 98(4): 2232 - 2243. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. L. Person and D. J. Perkel Pallidal Neuron Activity Increases during Sensory Relay through Thalamus in a Songbird Circuit Essential for Learning J. Neurosci., August 8, 2007; 27(32): 8687 - 8698. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. B. Spraker, H. Yu, D. M. Corcos, and D. E. Vaillancourt Role of Individual Basal Ganglia Nuclei in Force Amplitude Generation J Neurophysiol, August 1, 2007; 98(2): 821 - 834. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. R. Sadek, P. J. Magill, and J. P. Bolam A Single-Cell Analysis of Intrinsic Connectivity in the Rat Globus Pallidus J. Neurosci., June 13, 2007; 27(24): 6352 - 6362. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Spielman, L. O. Ramig, L. Mahler, A. Halpern, and W. J. Gavin Effects of an Extended Version of the Lee Silverman Voice Treatment on Voice and Speech in Parkinson's Disease Am J Speech Lang Pathol, May 1, 2007; 16(2): 95 - 107. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Elias, M. Joshua, J. A. Goldberg, G. Heimer, D. Arkadir, G. Morris, and H. Bergman Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus J. Neurosci., March 7, 2007; 27(10): 2525 - 2538. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Pasquereau, A. Nadjar, D. Arkadir, E. Bezard, M. Goillandeau, B. Bioulac, C. E. Gross, and T. Boraud Shaping of Motor Responses by Incentive Values through the Basal Ganglia J. Neurosci., January 31, 2007; 27(5): 1176 - 1183. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Leblois, T. Boraud, W. Meissner, H. Bergman, and D. Hansel Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci., March 29, 2006; 26(13): 3567 - 3583. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. S. Turner and M. E. Anderson Context-Dependent Modulation of Movement-Related Discharge in the Primate Globus Pallidus J. Neurosci., March 16, 2005; 25(11): 2965 - 2976. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Arkadir, G. Morris, E. Vaadia, and H. Bergman Independent Coding of Movement Direction and Reward Prediction by Single Pallidal Neurons J. Neurosci., November 10, 2004; 24(45): 10047 - 10056. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Wichmann and M. A. Kliem Neuronal Activity in the Primate Substantia Nigra Pars Reticulata During the Performance of Simple and Memory-Guided Elbow Movements J Neurophysiol, February 1, 2004; 91(2): 815 - 827. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. S. Turner, M. Desmurget, J. Grethe, M. D. Crutcher, and S. T. Grafton Motor Subcircuits Mediating the Control of Movement Extent and Speed J Neurophysiol, December 1, 2003; 90(6): 3958 - 3966. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. L. Rubchinsky, N. Kopell, and K. A. Sigvardt Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus-pallidal circuits PNAS, November 25, 2003; 100(24): 14427 - 14432. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Liotti, L.O. Ramig, D. Vogel, P. New, C.I. Cook, R.J. Ingham, J.C. Ingham, and P.T. Fox Hypophonia in Parkinson's disease: Neural correlates of voice treatment revealed by PET Neurology, February 11, 2003; 60(3): 432 - 440. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Anderson, N. Postupna, and M. Ruffo Effects of High-Frequency Stimulation in the Internal Globus Pallidus on the Activity of Thalamic Neurons in the Awake Monkey J Neurophysiol, February 1, 2003; 89(2): 1150 - 1160. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Hanson and D. Jaeger Short-Term Plasticity Shapes the Response to Simulated Normal and Parkinsonian Input Patterns in the Globus Pallidus J. Neurosci., June 15, 2002; 22(12): 5164 - 5172. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. D. Bevan, P. J. Magill, N. E. Hallworth, J. P. Bolam, and C. J. Wilson Regulation of the Timing and Pattern of Action Potential Generation in Rat Subthalamic Neurons In Vitro by GABA-A IPSPs J Neurophysiol, March 1, 2002; 87(3): 1348 - 1362. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Hanna-Pladdy, K. M. Heilman, and A. L. Foundas Cortical and subcortical contributions to ideomotor apraxia: Analysis of task demands and error types Brain, December 1, 2001; 124(12): 2513 - 2527. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Bosco and R. E. Poppele Proprioception From a Spinocerebellar Perspective Physiol Rev, April 1, 2001; 81(2): 539 - 568. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Gdowski, L. E. Miller, T. Parrish, E. K. Nenonene, and J. C. Houk Context Dependency in the Globus Pallidus Internal Segment During Targeted Arm Movements J Neurophysiol, February 1, 2001; 85(2): 998 - 1004. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. S. Turner and M. R. DeLong Corticostriatal Activity in Primary Motor Cortex of the Macaque J. Neurosci., September 15, 2000; 20(18): 7096 - 7108. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Nambu, H. Tokuno, I. Hamada, H. Kita, M. Imanishi, T. Akazawa, Y. Ikeuchi, and N. Hasegawa Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey J Neurophysiol, July 1, 2000; 84(1): 289 - 300. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. van Donkelaar, J. F. Stein, R. E. Passingham, and R. C. Miall Temporary Inactivation in the Primate Motor Thalamus During Visually Triggered and Internally Generated Limb Movements J Neurophysiol, May 1, 2000; 83(5): 2780 - 2790. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Boraud, E. Bezard, B. Bioulac, and C. E. Gross Ratio of Inhibited-to-Activated Pallidal Neurons Decreases Dramatically During Passive Limb Movement in the MPTP-Treated Monkey J Neurophysiol, March 1, 2000; 83(3): 1760 - 1763. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. W. Moran and A. B. Schwartz Motor Cortical Representation of Speed and Direction During Reaching J Neurophysiol, November 1, 1999; 82(5): 2676 - 2692. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. B. Schwartz and D. W. Moran Motor Cortical Activity During Drawing Movements: Population Representation During Lemniscate Tracing J Neurophysiol, November 1, 1999; 82(5): 2705 - 2718. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. D. Bevan and C. J. Wilson Mechanisms Underlying Spontaneous Oscillation and Rhythmic Firing in Rat Subthalamic Neurons J. Neurosci., September 1, 1999; 19(17): 7617 - 7628. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Zhang and T. J. Sejnowski A Theory of Geometric Constraints on Neural Activity for Natural Three-Dimensional Movement J. Neurosci., April 15, 1999; 19(8): 3122 - 3145. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. D. Bevan, P. A. C. Booth, S. A. Eaton, and J. P. Bolam Selective Innervation of Neostriatal Interneurons by a Subclass of Neuron in the Globus Pallidus of the Rat J. Neurosci., November 15, 1998; 18(22): 9438 - 9452. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. S. Turner, S. T. Grafton, J. R. Votaw, M. R. Delong, and J. M. Hoffman Motor Subcircuits Mediating the Control of Movement Velocity: A PET Study J Neurophysiol, October 1, 1998; 80(4): 2162 - 2176. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. B. Bhat and J. N. Sanes Cognitive Channels Computing Action Distance and Direction J. Neurosci., September 15, 1998; 18(18): 7566 - 7580. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
